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The Genera Melanothamnus Bornet & Falkenberg and Vertebrata S.F

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European Journal of Phycology ISSN: 0967-0262 (Print) 1469-4433 (Online) Journal homepage: http://www.tandfonline.com/loi/tejp20 The genera Melanothamnus Bornet & Falkenberg and Vertebrata S.F. Gray constitute well-defined clades of the red algal tribe Polysiphonieae (Rhodomelaceae, Ceramiales) Pilar Díaz-Tapia, Lynne McIvor, D. Wilson Freshwater, Heroen Verbruggen, Michael J. Wynne & Christine A. Maggs To cite this article: Pilar Díaz-Tapia, Lynne McIvor, D. Wilson Freshwater, Heroen Verbruggen, Michael J. Wynne & Christine A. Maggs (2017) The genera Melanothamnus Bornet & Falkenberg and Vertebrata S.F. Gray constitute well-defined clades of the red algal tribe Polysiphonieae (Rhodomelaceae, Ceramiales), European Journal of Phycology, 52:1, 1-30, DOI: 10.1080/09670262.2016.1256436 To link to this article: http://dx.doi.org/10.1080/09670262.2016.1256436 View supplementary material Published online: 01 Feb 2017. Submit your article to this journal Article views: 181 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tejp20 Download by: [UNAM Ciudad Universitaria] Date: 04 May 2017, At: 14:07 EUROPEAN JOURNAL OF PHYCOLOGY, 2017 VOL. 52, NO. 1, 1–30 http://dx.doi.org/10.1080/09670262.2016.1256436 The genera Melanothamnus Bornet & Falkenberg and Vertebrata S.F. Gray constitute well-defined clades of the red algal tribe Polysiphonieae (Rhodomelaceae, Ceramiales) Pilar Díaz-Tapiaa,b,c, Lynne McIvord, D. Wilson Freshwatere, Heroen Verbruggen c, Michael J. Wynnef and Christine A. Maggs b,d aBioCost Research Group, Universidad de A Coruña, 15071, A Coruña, Spain; bFaculty of Science and Technology, Bournemouth University, Talbot Campus, Poole, Dorset BH12 5BB, UK; cSchool of BioSciences, University of Melbourne, Victoria 3010, Australia; dSchool of Biological Sciences, Queen’s University Belfast, Medical Biology Centre, BT9 7BL, Northern Ireland; eCenter for Marine Science, University of North Carolina at Wilmington, 5600 Marvin Moss Lane, Wilmington, NC 28409, USA; fDepartment of Ecology and Evolutionary Biology and Herbarium, University of Michigan Ann Arbor, MI 48109, USA ABSTRACT Polysiphonia is the largest genus of red algae, and several schemes subdividing it into smaller taxa have been proposed since its original description. Most of these proposals were not generally accepted, and currently the tribe Polysiphonieae consists of the large genus Polysiphonia (190 species), the segregate genus Neosiphonia (43 species) and 13 smaller genera (< 10 species each). In this paper, phylogenetic relationships of the tribe Polysiphonieae are analysed, with particular emphasis on the genera Carradoriella, Fernandosiphonia, Melanothamnus, Neosiphonia, Polysiphonia sensu stricto, Streblocladia and Vertebrata. We evaluated the consistency of 14 selected morphological characters in the identified clades. Based on molecular phylogenetic (rbcL and 18S genes) and morphological evidence, two speciose genera are recognized: Vertebrata (including the type species of the genera Ctenosiphonia, Enelittosiphonia, Boergeseniella and Brongniartella) and Melanothamnus (including the type species of the genera Fernandosiphonia and Neosiphonia). Both genera are distinguished from other members of the Polysiphonieae by synapomorphic characters, the emergence of which could have provided evolutionarily selective advantages for these two lineages. In Vertebrata trichoblast cells are multinucleate, possibly associated with the development of extraordinarily long photoprotective trichoblasts. Melanothamnus has 3-celled carpogonial branches and plastids lying exclusively on radial walls of the pericentral cells, which similarly may improve resistance to damage caused by excessive light. Other relevant characters that are constant in each genus are also shared with other clades. The evolutionary origin of the genera Melanothamnus and Vertebrata is estimated as 75.7–95.78 and 90.7–138.66 Ma, respectively. Despite arising in the Cretaceous, before the closure of the Tethys Seaway, Melanothamnus is a predominantly Indo-Pacific genus and its near-absence from the north-eastern Atlantic is enigmatic. The nomenclatural implications of this work are that 46 species are here transferred to Melanothamnus, six species are transferred to Vertebrata, and 13 names are resurrected for Vertebrata. ARTICLE HISTORY Received 1 October 2016; Revised 28 October 2016; Accepted 30 October 2016 KEYWORDS Biogeography; evolution; molecular systematics; morphology; phylogeny; Polysiphonia; red algae; time calibration Introduction the most speciose is the Polysiphonieae with over 300 species in 15 currently recognized genera (Guiry & The Rhodomelaceae Areschoug is the largest family Guiry, 2016). of red algae, currently including more than 1000 Within the Polysiphonieae the genus Polysiphonia species (Guiry & Guiry, 2016). It consists of the tribes Greville (1824), nom. cons., has representatives Amansieae Schmitz (1889), Bostrychieae Falkenberg throughout the world, in the majority of photic mar- (1901), Chondrieae Schmitz & Falkenberg (1897), ine benthic habitats including brackish ones (e.g. Herposiphonieae Schmitz & Falkenberg (1897), Hollenberg, 1942, 1944, 1968a, 1968b; Womersley, Heterocladieae Falkenberg (1901), Laurencieae 1979; Maggs & Hommersand, 1993; Lam et al., Schmitz (1889), Lophothalieae Schmitz & 2013). Polysiphonia is poorly circumscribed, and has Falkenberg (1897), Neotenophyceae Kraft & I.A. remained in a state of taxonomic flux since its origi- Abbott (2002), Pleurostichidieae (Hommersand, nal description. Numerous schemes for subdividing 1963), Polysiphonieae Schmitz (1889), Polyzonieae this large and morphologically diverse genus into Schmitz & Falkenberg (1897), Pterosiphonieae smaller and more manageable groups have been pro- Falkenberg (1901), Rhodomeleae Schmitz & posed (e.g. Segi, 1951; Hollenberg, 1968a, 1968b), Falkenberg (1897), Sonderelleae L.E.Phillips (2001) based mostly on the number of periaxial cells, either and Streblocladieae nom. nud. (Hommersand, 1963; four (subgenus Oligosiphonia) or more than four Kraft & Abbott, 2002; Womersley, 2003), of which CONTACT Pilar Díaz-Tapia [email protected] © 2017 British Phycological Society 2 P. DÍAZ-TAPIA ET AL. (subgenus Polysiphonia). These schemes have gener- relationship between Neosiphonia species and ally been rejected and several generic names (e.g. Melanothamnus somalensis, the type species of the Orcasia Kylin (1941), based on Polysiphonia senticu- genus Melanothamnus Bornet & Falkenberg, which losa Harvey) are currently regarded as synonyms of was regarded as incertae sedis (Falkenberg, 1901). Polysiphonia. However, despite having been sub- Given the taxonomic and nomenclatural complex- sumed within Polysiphonia in most classification ity within the Polysiphonieae, our aims were to re- schemes, Vertebrata S.F.Gray (1821) is currently evaluate the morphological features of Neosiphonia recognized as a monospecific genus containing only and Vertebrata in relation to those of the type species, V. lanosa. Fernandosiphonia, Streblocladia, Carradoriella, The segregate genus Neosiphonia M.-S.Kim & I.K. Melanothamnus and Polysiphonia sensu stricto within Lee (Kim & Lee, 1999) has been widely accepted and a phylogenetic analysis of the Polysiphonieae using is now the second largest in the Polysiphonieae sequences of the plastid-encoded rbcL gene and the (Guiry & Guiry, 2016). Neosiphonia (type species: N. ribosomal DNA 18S gene (SSU). We surveyed within flavimarina from Korea) is characterized by the fol- the Polysiphonieae the distribution of a striking char- lowing features: (1) thalli erect with a main axis acteristic of the ‘Polysiphonia japonica complex’, the bearing branches; (2) branches or trichoblasts formed position of plastids on radial walls of the periaxial on every segment; (3) rhizoids cut off from pericen- cells and their absence from the outer walls such that tral cells; (4) carpogonial branches 3-celled; (5) sper- nuclei are clearly visible after staining (Maggs & matangial branches formed on a branch of modified Hommersand, 1993; McIvor et al., 2001). Likewise, trichoblasts; (6) tetrasporangia in spiral arrangement we analysed the multinucleate vs. uninucleate char- (Kim & Lee, 1999). These features contrast markedly acter of trichoblast cells, which seems to be taxono- with the key characters of Polysiphonia sensu stricto, mically significant (Maggs & Hommersand, 1993). exemplified by the type species P. stricta: prostrate axes with rhizoids in open connection with pericen- tral cells; carpogonial branches 4-celled; spermatan- Materials and methods gial branches borne directly on axes; tetrasporangia in Field collections, morphological studies and straight rows (Kim et al., 2000). In addition to literature review describing the new species N. flavimarina, Kim & Lee (1999) also transferred 11 species of Samples of Polysiphonieae (Table S1) were collected Polysiphonia to Neosiphonia, all based on material from European Atlantic coasts, New Zealand, from Korea, and there are 43 currently recognized Australia, Taiwan, Japan, Chile, USA, South Africa species (Guiry & Guiry, 2016), not all of which exhi- and Oman and processed fresh, desiccated in silica bit the six key characters of Neosiphonia listed above. gel or preserved in ethanol. Kim & Lee (1999) considered Neosiphonia (also Type material of Fernandosiphonia unilateralis was referred to as the ‘Polysiphonia japonica complex’ obtained
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    “A língua e a escrita não chegam para descrever todas as maravilhas do mar” Cristóvão Colombo Agradecimentos Aqui agradeço a todas as pessoas que fizeram parte deste meu percurso de muita alegria, trabalho, desafios e acima de tudo aprendizagem: Ao meu orientador, Professor Doutor Leonel Pereira por me ter aceite como sua discípula, guiando-me na execução deste trabalho. Agradeço pela disponibilidade sempre prestada, pelos ensinamentos, conselhos e sobretudo pelo apoio em altura mais complicadas. Ao Professor Doutor Ignacio Bárbara por me ter auxiliado na identificação e confirmação de algumas espécies de macroalgas. E ao Professor Doutor António Xavier Coutinho por me ter cedido gentilmente, diversas vezes, o seu microscópio com câmara fotográfica incorporada, o que me permitiu tirar belas fotografias que serviram para ilustrar este trabalho. Ao meu colega Rui Gaspar pelo interesse demonstrado pelo meu trabalho, auxiliando-me sempre que necessário e também pela transmissão de conhecimentos. Ao Sr. José Brasão pela paciência e pelo auxílio técnico no tratamento das amostras. Em geral, a todos os meus amigos que me acompanharam nesta etapa de estudante de Coimbra e que me ajudaram a sê-lo na sua plenitude, e em particular a três pessoas: Andreia, Rita e Vera pelas nossas conversas e pelo apoio que em determinadas etapas foram muito importantes e revigorantes. Às minhas últimas colegas de casa, Filipa e Joana, pelo convívio e pelo bom ambiente “familiar” que se fazia sentir naquela casinha. E como os últimos são sempre os primeiros, à minha família, aos meus pais e à minha irmã pelo apoio financeiro e emocional, pela paciência de me aturarem as “neuras” e pelo acreditar sempre que este objectivo seria alcançado.
  • Widely Distributed Red Algae Often Represent Hidden Introductions, Complexes of Cryptic Species Or Species with Strong Phylogeographic Structure1

    Widely Distributed Red Algae Often Represent Hidden Introductions, Complexes of Cryptic Species Or Species with Strong Phylogeographic Structure1

    J. Phycol. *, ***–*** (2018) © 2018 Phycological Society of America DOI: 10.1111/jpy.12778 WIDELY DISTRIBUTED RED ALGAE OFTEN REPRESENT HIDDEN INTRODUCTIONS, COMPLEXES OF CRYPTIC SPECIES OR SPECIES WITH STRONG PHYLOGEOGRAPHIC STRUCTURE1 Pilar Dıaz-Tapia 2 Coastal Biology Research Group, Faculty of Sciences and Centre for Advanced Scientific Research (CICA), University of A Coruna~ 15071, A Coruna,~ Spain School of BioSciences, University of Melbourne, Melbourne, Victoria 3010, Australia Christine A. Maggs Portaferry Marine Laboratory, Queen’s University Belfast, Belfast BT22 1PF, UK Erasmo C. Macaya Laboratorio de Estudios Algales (ALGALAB), Departamento de Oceanografıa, Facultad de Ciencias Naturales y Oceanograficas, Universidad de Concepcion, Concepcion, Chile Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Larrondo, 1281, Coquimbo, Chile Centro FONDAP de Investigaciones en Dinamica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Valdivia, Chile and Heroen Verbruggen School of BioSciences, University of Melbourne, Melbourne, Victoria 3010, Australia Despite studies suggesting that most seaweeds are spinifera). This study shows that widely distributed poor dispersers, many red algal species are reported species are the exception in marine red algae, unless to have circumglobal distributions. Such distributions they have been spread by humans. have mostly been based on morphological iden- Key index words: Herposiphonieae; introductions; new tifications, but molecular data have revealed a range record; phylogeography; Polysiphonieae; Pterosipho- of issues with morphologically defined species nieae; rbcL; Rhodomelaceae; species boundaries; spe- boundaries. Consequently, the real distribution of cies complexes such reportedly circumglobal species must be questioned. In this study, we analyzed molecular data sets (rbcL gene) of nine species in the Rhodo- melaceae for which samples were available from Phylogeography of marine organisms is influ- widely spaced geographical locations.